Vaccination coverage among older adults: a population-based study in India

Abstract Objective To estimate the prevalence and explore the predictors of vaccine uptake among older adults in India. Methods We used data from the national Longitudinal Ageing Study in India, a national household survey conducted during 2017–2018. Based on interviewees’ self-reports, we calculated population-weighted estimates of the uptake of influenza, pneumococcal, typhoid and hepatitis B vaccines among 64 714 Indian adults aged 45 years or older. We performed multivariable binary logistic regression analysis to examine the sociodemographic and health-related predictors of uptake of the vaccinations. Findings The coverage of each of the studied vaccinations was less than 2%. The estimated percentages of respondents reporting ever being vaccinated were 1.5% (95% confidence interval, CI: 1.4–1.6) for influenza, 0.6% (95% CI: 0.6–0.7) for pneumococcal disease, 1.9% (95% CI: 1.8–2.0) for typhoid and 1.9% (95% CI: 1.8–2.0) for hepatitis B. Vaccine uptake was higher among respondents with cardiovascular disease, diabetes or lung disease than those without any of these conditions. Uptake of influenza vaccine was higher among those with lung disease, while hepatitis B vaccine uptake was higher among those with cardiovascular disease or diabetes. Male sex, urban residence, wealthier household, more years of schooling, existing medical conditions and sedentary behaviours were significant predictors of vaccine uptake. Conclusion Targeted policies and programmes are needed for improving the low vaccination coverage among older adults in India, especially among those with chronic diseases. Further research could examine vaccine access, vaccine hesitancy, and vaccine-related information and communication channels to older adults and their health-care providers.


Introduction
Both the Global Vaccine Action Plan endorsed at the 2012 World Health Assembly 1 and the Immunization Agenda 2030 endorsed in 2021 proposed a life-course approach to immunization to fight vaccine-preventable diseases. 2 The coronavirus disease 2019 (COVID-19) pandemic has also underlined the importance of robust vaccination systems for control of vaccine-preventable diseases among older adults. In 2009 the Association of Physicians in India drew attention to the substantial burden of morbidity, disability and mortality due to infectious diseases among older adults in the country. 3 The association recommended that vaccination was the most beneficial and cost-effective way to prevent and control infectious diseases in adults. Identification of vulnerable groups and the development of vaccination strategies for older people are therefore needed.
As reported in the World Health Organization's (WHO) 2012 Global report for research on infectious diseases of poverty, diseases such as pneumonia, malaria, respiratory diseases, tuberculosis and typhoid pose a significant burden on low-and middle-income countries. 4 Studies have shown that influenza and pneumococcal disease cause serious complications, especially in older adults with chronic illnesses. 5 According to India's National Centre for Disease Control, there were nearly 115 630 cases of H1N1 seasonal influenza in India between 2010 and 2017, accounting for 8685 deaths. 6 Pneumococcal disease is a significant cause of bacterial pneumonia. 7 The United States Centers for Disease Control and Prevention reported that pneumococcal pneumonia, resulting in one death in 20 adults (5%), has a high mortality in older adults. 8 Likewise, acute hepatitis B virus (HBV) infection can cause severe illness and death and can lead to chronic HBV infec-tion or liver cancer. 9,10 The burden of HBV in India falls in the intermediate endemicity zone (prevalence of 2-7%, an average of 4%), affecting about 50 million people. The prevalence of HBV infection is higher in adults with diabetes. 11 Typhoid is also a major burden on India's public health system. In 2017, India had 6.6 million typhoid cases, accounting for 66 439 deaths. 12 In 2008, the incidence of typhoid (493.5 cases per 100 000 per year) in India was the highest worldwide, followed by Pakistan, Indonesia, China and Viet Nam. 13 Together, these infections are the leading causes of morbidity in older adults, resulting in hospitalization and death.
Due to declining fertility and increasing life expectancy, India is seeing a steady increase in the proportion of older people in the population. According to the 2011 Indian census, the adult population aged 45 years and older was 222 797 316 (18.4%) of the Indian population of 1 210 854 977. This figure is expected to rise to 40% (655 million people) by 2050. 14,15 Besides the demographic transition, epidemiological transition has shifted the overall burden of disease towards older adults. Although chronic noncommunicable diseases have emerged as a primary concern, infectious diseases among such a large older population still pose a significant challenge to the Indian public health system. 16 Studies on vaccination coverage among older adults are limited and mostly come from high-income countries. Researchers have reported that in people 65 years or older, seasonal influenza vaccination was received by more than 75% (8 363 467) of 10 341 592 people in the United Kingdom of Great Britain and Northern Ireland, 65% of 5332 people in the United States of America and 70% of 789 people surveyed in Canada. [17][18][19] In comparison, a study from China reported that only 7.4% of 5414 people aged 60 years or older had received influenza vaccination. 20 Many sociodemographic and health Research Vaccination coverage among older adults, India Ali Abbas Rizvi & Abhishek Singh factors influence vaccine uptake among older adults. 21,22 A systematic review of data from 12 countries found that older adults who received pandemic A(H1N1) influenza vaccination were more likely to be of higher education status, to have comorbidities and to have belief in vaccine efficacy. 21 Another study found that previous vaccination history and physician recommendations were associated with vaccine uptake in older adults. 22 Here, we aimed to analyse the uptake of four vaccines recommended for adults (influenza, pneumococcal, typhoid and hepatitis B) and the factors associated with their uptake among older adults in India. Such studies are essential for planning and implementing strategies to improve vaccination coverage among older adults in this large and diverse country. In addition, by identifying the underlying predictors of vaccination, we may be able to target vulnerable groups for future programme interventions.

Data source
We used data from the first wave of the Longitudinal Ageing Study in India conducted during 2017-2018. The study is a nationally representative survey of India's health, economic, and social determinants and consequences of ageing. The study comprised interviews with 72 250 adults aged 45 years and older, including their spouses irrespective of age, across 30 states and six union territories of India. The response rate to the survey was 87.3% (72 250 out of 82 650 people approached). The study used a multistage, stratified, area-probability cluster-sampling design to collect data from both rural and urban areas. The details of the sampling design, survey instruments, fieldwork, data collection and processing are available elsewhere. 23 We analysed information collected from 64 714 adults aged 45 years or older.
Ethical approval was not required for the study as we used publicly available data from a longitudinal study that used standard procedures for data collection with ethically approved guidelines and informed consent from participants.

Data collection
The dependent variables were ever uptake of influenza, pneumococcal, ty-phoid or hepatitis B vaccines. Interviewees in the Longitudinal Ageing Study were asked: "Have you ever received any immunizations for adults, such as the influenza vaccine, pneumococcal vaccine, hepatitis B vaccine, or typhoid vaccine?" All the dependent variables were binary, with the response categories as Yes or No.
We extracted data on the sociodemographic characteristics of respondents: age (45-59, 60-69, 70-79, ≥ 80 years); sex (male, female); marital status (currently married, widowed, other); length of schooling (none, up to 5 years, 5-9 years, ≥ 10 years); working status (currently working, not working); social group (scheduled caste or tribe, other backward class, other); religion (Hindu, Muslim, other); wealth quintiles (poorest, poorer, middle, richer, richest); urban or rural area; and geographical region of residence (north, central, east, north-east, west, south). The Longitudinal Ageing Study reports wealth quintiles estimated from total monthly household expenditure. Scheduled castes or tribes and other backward classes are the constitutionally recognized groups of disadvantaged and deprived communities in India, and the Other category consisted of those who do not belong to these categories. The Other religion category included Christian, Sikh, other religions and no religion.
We also extracted data on healthrelated factors, including hospitalization in the past 12 months (yes, no); type of health care facility (public, private); physical activity (every day, sometimes, none); currently smoking (yes, no); ever alcohol consumption (yes, no); and having chronic disease(s) (yes, no). We considered sport or vigorous activity as a physical activity. Chronic diseases included at least one of hypertension, diabetes, cancer, lung disease, heart disease and stroke.

Data analysis
First, we estimated the prevalence of uptake of the four types of vaccination among the respondents. Then we examined the prevalence of uptake of each type of vaccination by the respondents' sociodemographic and health-related characteristics. Finally, we estimated four separate multivariable binary logistic regressions to study the factors associated with vaccine uptake. The statistically significant difference between the estimates was set at 5% level of significance. We used the survey weights given in the Longitudinal Ageing Study data set to estimate the prevalence of vaccination uptake for population size, adjusting for the complex design of the study to generate nationally representative estimates. We carried out the analysis using Stata version 14.0 (Stata Corp., College Station, USA).  Table 1 shows the population-weighted numbers and estimated percentages of respondents who reported ever receiving the studied vaccines. Uptake was less than 2% for each of the vaccines.

Vaccination uptake
An estimated 1315 respondents had received influenza vaccination, an overall uptake of 1.5% (95% confidence interval, CI: 1.4-1.6). Influenza vaccine uptake was slightly higher among men and among those who were not currently married or widowed, were not working, were neither Hindu nor Muslim, were in the wealthiest quintile, had been hospitalized in the last 12 months or had at least one chronic illness. Influenza vaccination uptake was highest in the south region of India followed by the north region.

Research
Vaccination coverage among older adults, India Ali Abbas Rizvi & Abhishek Singh CI: 0.6-0.7). The uptake of pneumococcal vaccine was higher with older age and more years of schooling. Pneumococcal vaccine uptake was also higher among respondents who were working, were not of scheduled tribes, scheduled castes or other backward classes, were wealthier, had a chronic illness, were from the north region and were neither Hindu nor Muslim. Vaccination for typhoid or hepatitis B was received by 1518 and 1933 respondents, respectively, showing an uptake prevalence of 1.9% (95% CI: 1.8-2.0) for each vaccine. The uptake of typhoid and hepatitis B vaccines also show similar patterns across the studied variables, except for urban or rural area. The prevalence of typhoid and hepatitis B vaccination was higher among older adults who were currently married, had 10 or more years of schooling, did not belong to scheduled tribes, scheduled castes or other backward classes, were neither Hindu nor Muslim, were wealthier, were from the north region, had a history of hospitalization, used private health-care facilities and had at least one chronic disease.
Vaccine uptake was higher among respondents with cardiovascular disease, diabetes or lung disease than those without any of these conditions (Table 1;  Table 2). For example, estimated influenza vaccine uptake was 2.4% (95% CI: 1.9-2.9) among those with lung disease compared with 1.1% (95% CI: 1.0-1.2) among those with no chronic illness.

Multivariable logistic regression
In our multivariable logistic regression analysis, the age of the respondents was not associated with uptake of any of the four types of vaccination (

Discussion
The uptake of the studied vaccines by older adults in India was considerably lower than that of higher income coun-tries. 24 Vaccination uptake ranged from 0.6% for pneumococcal vaccine to 1.9% for typhoid and hepatitis B vaccines. A 2020 study from China estimated a low, but slightly higher, prevalence of influenza vaccination among older adults (1651 out of 74 484 respondents; 2.4%). 25 The low uptake may be explained by a lack of awareness and knowledge about vaccination for infectious diseases in adults, as noted by studies in India, Saudi Arabia and the USA. [26][27][28][29] The study conducted in India found that out of 149 patients, only 2% and 0.7% had received influenza and pneumococcus vaccination, respectively. 26 In a study of 832 diabetic patients admitted to a university hospital in Saudi Arabia, less than 40% of patients thought they were at a high risk of acquiring an infectious disease. 29 Vaccination uptake among older adults in India varied by sociodemographic and health characteristics. Male sex, urban residence, existing medical conditions, more years of schooling and not engaging in physical activities were significant predictors of vaccine uptake. These findings are consistent with previous studies conducted in China and the USA among older adult populations. 18,27,30 Higher vaccination coverage in urban areas was also evident in recent studies conducted in China. 25,31 The uptake of influenza and pneumococcal vaccines was higher among older adults having lung diseases than those with other morbidities. Older adults with cardiovascular diseases were more likely to have received typhoid and hepatitis B vaccinations. A history of hospitalization was strongly linked to uptake of typhoid and hepatitis B vaccinations in our study. This finding is consistent with studies showing that health-care providers play an important role in motivating older adults to take up vaccination. 32,33 For each of the four vaccinations, older adults from the richest wealth quintile households were significantly more likely to report being vaccinated than their counterparts from the poorest wealth quintile households. This finding is consistent with studies conducted in India and Poland that reported poor economic status as the most common barrier to vaccine uptake by adults. 26,34 This finding is important given that poor people are at a higher risk of vaccine-preventable diseases and are disproportionally vulnerable to the economic impact of these diseases. Furthermore, expenditure on vaccina-tions among older adults is mainly funded out-of-pocket. 35 In low-and middle-income countries many factors can impede the delivery of life-course immunization beyond childhood. These factors include an absence of policies for promoting adult vaccination, competing health priorities, lack of financing for health, heterogeneous populations and a dearth of research-based evidence. Fortunately, the Indian government has acted towards a healthy ageing approach by including special provisions for older adults in the health and wellness centres being opened across the country. 36 Studies conducted in China and the USA have found regional variations in vaccine uptake by adults. 25,27 In our study, the prevalence of uptake of pneumococcal, typhoid and hepatitis B vaccinations were highest in the north region of India. A higher prevalence of infectious diseases in the north region may be associated with the higher vaccination coverage. 37 On the other hand, higher influenza vaccination coverage in the south region of India may be confounded by the higher prevalence of diabetes in the region. 16 We also found a high vaccination coverage of hepatitis B in the north-east states. This could be due to the high prevalence of hepatitis B in the tribal-dominated region. 38 Vaccine-preventable death has been used in several studies to measure the efficacy of the vaccination among older adults, as measured by uptake of childhood vaccination. However, vaccinepreventable disability might be a better indicator to assess the effectiveness of vaccines among older adults. 39 Increasing vaccine uptake among older adults requires better availability and access to vaccines and improved financing and monitoring of vaccination systems. Engaging civil society and a proper campaigning strategy for vaccination may help counteract vaccine hesitancy among the public. The COVID-19 pandemic has opened a window of opportunity to build a mechanism for promoting adult immunization and a system to deliver the vaccines. Also, a life-course approach may be adopted for the needs of different groups of people in different regions of a country. Moreover, public and private health insurance policies may include vaccination for older adults with and without comorbidities.  and universal health coverage agendas into Immunization Agenda 2030 and empowering low-and middle-income countries to develop adult immunization programmes. 40 This study has some limitations. Our analysis was based on respondents' self-reports which may be subject to recall bias. Second, our analysis was based on cross-sectional data and hence causal relationships cannot be established. Third, we did not explore the reasons for low vaccine uptake, access to vaccines and vaccine hesitancy among older adults in India. While influenza vaccine is valid only for one year, hepatitis B vaccine should be given as a series of two, three or four doses, depending on the vaccine manufacturer. For typhoid vaccine, a booster dose is needed every 5 years for people who remain at risk. We could not include vaccination time periods, doses or booster doses in our analysis due to lack of these data in the Longitudinal Ageing Study in India.
Vaccination coverage among older adults, India Ali Abbas Rizvi & Abhishek Singh